Applied Microbiology and Biotechnology

, Volume 100, Issue 24, pp 10627–10636 | Cite as

Degradation of phenanthrene by Novosphingobium sp. HS2a improved plant growth in PAHs-contaminated environments

  • Sara Rodriguez-Conde
  • Lázaro Molina
  • Paola González
  • Alicia García-Puente
  • Ana Segura
Environmental biotechnology
First Online:
Received:
Revised:
Accepted:

Abstract

At the same time that the European Union (EU) policy recommend to direct efforts towards reductions of heavy metals, polycyclic aromatic hydrocarbons (PAHs) and mining residues, there is the need to increase the cultivable areas within Europe to cope with the increasing demands for food and energy crops. Bioremediation is a good technique for the restoration of contaminated soils; however, it has not been used extensively because of the variability of the outcome. This variability is frequently due to a bad establishment of foreign degrading populations in soil. We have demonstrated that Novosphingobium sp. HS2aR (i) is able to compete with other root colonizers and with indigenous bacteria, (ii) is able to establish in high numbers in the contaminated environments and (iii) is able to remove more than 90 % of the extractable phenanthrene in artificially contaminated soils. Furthermore, we have demonstrated that the capacity to remove phenanthrene is linked to the ability to promote plant growth in contaminated environments. The fact that the presence of Novosphingobium sp. HS2aR improves the growth of plants in contaminated soil suggests that it may be a useful strain for utilization in amelioration of soil quality while improving the growth of economically important energy crops, thus adding value to the bioremediation strategy.

Keywords

Bioremediation Novosphingobium Polycyclic aromatic hydrocarbons Plant growth promoting bacteria 
This is a preview of subscription content, log in to check access.

Notes

Acknowledgments

This study has been supported by research grants from the Spanish Ministry of Science and Innovation (BIO2010-16668) and the Andalusian Regional Government (Junta de Andalucía) (P06-CVI-01767).

Compliance with ethical standards

Conflict of interests

The authors declare that they have no conflict of interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2016_7892_MOESM1_ESM.pdf (300 kb)
ESM 1 (PDF 300 kb)

References

  1. Abril MA, Michán C, Timmis KN, Ramos JL (1989) Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate of the pathway. J Bacteriol 171:6782–6790CrossRefPubMedPubMedCentralGoogle Scholar
  2. Böltner D, Godoy P, Muñoz-Rojas J, Duque E, Moreno-Morillas S, Sánchez L, Ramos JL (2008) Rhizoremediation of lindane by root-colonizing Sphingomonas. Microb Biotechnol 1:87–93PubMedGoogle Scholar
  3. Bouchez T, Patureau D, Dabert P, Juretschko S, Doré J, Delgenès P, Moletta R, Wagner M (2000) Ecological study of a bioaugmentation failure. Environ Microbiol 2:179–190CrossRefPubMedGoogle Scholar
  4. Cavalca L, Rao MA, Bernasconi S, Colombo M, Andreoni V, Gianfreda L (2008) Biodegradation of phenanthrene and analysis of degrading cultures in the presence of a model organo-mineral matrix and of a simulated NAPL phase. Biodegradation 19(1):13CrossRefGoogle Scholar
  5. Demanèche S, Meyer C, Micoud J, Louwagie M, Willison JC, Jouanneau Y (2004) Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:6714–6725CrossRefPubMedPubMedCentralGoogle Scholar
  6. Donnelly PK, Hegde RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–984CrossRefGoogle Scholar
  7. Escalante-Espinosa E, Gallegos-Martínez ME, Favela-Torres E, Gutierrez-Rojas M (2005) Improvement of the hydrocarbon phytoremediation rate by Cyperus laxus Lam, inoculated with a microbial consortium in a model system. Chemosphere 59:405–413CrossRefPubMedGoogle Scholar
  8. Gilbert ES, Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol 63:1933–1938PubMedPubMedCentralGoogle Scholar
  9. Graj W, Lisiecki P, Szulc A, Chrzanowski Ł, Wojtera-Kwiczor J (2013) Bioaugmentation with petroleum-degrading consortia has a selective growth-promoting impact on crop plants germinated in diesel oil-contaminated soil. Water Air Soil Pollut 224:1676CrossRefPubMedPubMedCentralGoogle Scholar
  10. Jones A, Panagos P, Barcelo S, Bouraoui F, Bosco C, Dewitte O, Garcid C, Erhard M, Hervás J, Hiederer R, Jeffery S, Lükewille A, Marmo L, Montanarella L, Olazábal C, Petersen J-E, Penizek V, Strassburger T, Tóth G, Van Den Eeckhaut M, Van Liedekerke M, Verheijen F, Viestova E, Yigini Y (2012) The State of Soil In Europe. JRC reference reports. https://biobs.jrc.ec.europa.eu/sites/default/files/generated/files/documents/JRC%20Report%20The%20State%20of%20Soil%20in%20Europe%202012.pdf
  11. Kirk JL, Klironomos JN, Lee H, Trevors JT (2005) The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environ Pollution 133:455–465CrossRefGoogle Scholar
  12. Kuiper I, Lagendijk EL, Pickford R, Derrick JP, Lamers GEM, Thomas-Oates JE, Lugtenberg BJJ, Bloemberg GV (2004) Characterization of two Pseudomonas putida lipopeptide biosurfactants, putisolvin I and II, which inhibit biofilm formation and break down existing biofilms. Mol Microbiol 51:97–113CrossRefPubMedGoogle Scholar
  13. Leigh MB, Fletcher JS, Fu X, Schmitz FJ (2002) Root turnover: an important source of microbial substrates in rhizosphere remediation of recalcitrant contaminants. Environ Sci Technol 36:1579–1583CrossRefPubMedGoogle Scholar
  14. Leys NMEJ, Ryngaer A, Bastiaens L, Verstraete W, Top EM, Springael D (2004) Occurrence and phylogenetic diversity of Sphingomonas strains in soils contaminated with polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:1944–1955CrossRefPubMedPubMedCentralGoogle Scholar
  15. Miller J (1972) Experiments in molecular genetics. Cold Spring Harbor, New YorkGoogle Scholar
  16. Molina L, Ramos C, Duque E, Ronchel MC, Garcöla JM, Wyke L, Ramos JL (2000) Survival of Pseudomonas putida KT2440 in soil and in the rhizosphere of plants under greenhouse and environmental conditions. Soil Biol Biochem 32:315–321CrossRefGoogle Scholar
  17. Mulla SI, Wang H, Sun Q, Hu A, Yu C-P (2016) Characterization of triclosan metabolism in Sphingomonas sp. strain YL-JM2C. Sci Rep 6:21965CrossRefPubMedPubMedCentralGoogle Scholar
  18. Murherjee AK, Bordoloi NK (2011) Bioremediation and reclamation of soil contaminated with petroleum oil hydrocarbons by exogenously seeded bacterial consortium: a pilot-scale study. Environ Pollut Res 18:471–478CrossRefGoogle Scholar
  19. Pandey J, Chauhan A, Jain RK (2009) Integrative approaches for assesing the ecological sustainability of in situ bioremediation. FEMS Microbiol Rev 33:324–375CrossRefPubMedGoogle Scholar
  20. Pinyakong O, Habe H, Supaka N, Pinpanichkarn P, Juntongjin K, Yoshida T, Furihata K, Nojiri H, Yamane H, Omori T (2000) Identification of novel metabolites in the degradation of phenanthrene by Sphingomonas sp. strain P2. FEMS Microbiol Lett 191:115–121CrossRefPubMedGoogle Scholar
  21. Prentki P, Krisch HM (1984) In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303–313CrossRefPubMedGoogle Scholar
  22. Rentz JA, Alvarez PJJ, Schnoor JL (2004) Repression of Pseudomonas putida phenanthrene-degrading activity by plant root extracts and exudates. Environ Microbiol 6:574–583CrossRefPubMedGoogle Scholar
  23. Reynoso-Cuevas L, Gallegos-Martínez ME, Cruz-Sosa F, Gutiérrez-Rojas M (2008) In vitro evaluation of germination and growth of five plant species on medium supplemented with hydrocarbons associated with contaminated soils. Bioresour Technol 99:6379–6385CrossRefPubMedGoogle Scholar
  24. Romine MF, Stillwell LC, Wong K-K, Thurston SJ, Sisk EC, Sensen C, Gaasterland T, Fredrickson JF, Saffer JD (1999) Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol 181:1585–1602PubMedPubMedCentralGoogle Scholar
  25. Schuler L, Jouanneau Y, Chadhain SMN, Meyer C, Pouli M, Zylstra GJ, Hols P, Agathos S (2009) Characterization of a ring-hydroxylating dioxygenase from phenanthrene-degrading Sphingomonas sp. strain LH128 able to oxidize benz[a]anthracene. Appl Microbiol Biotechnol 83:465–475CrossRefPubMedGoogle Scholar
  26. Shi T, Fredrickson JK, Balkwill DL (2001) Biodegradation of polycyclic aromatic hydrocarbons by Sphingomonas strains isolated from the terrestrial subsurface. J Ind Microbiol Biotechnol 26:283–289CrossRefPubMedGoogle Scholar
  27. Spaink HP, Okker RJH, Wijffelman CA, Pees E, Lugtenberg BJJ (1987) Promoters in the nodulation of the Rhizobium leguminosarum Sym plasmid pRL1J1. Plant Mol Biol 9:27–39CrossRefPubMedGoogle Scholar
  28. Sverdrup LE, Krogh PH, Nielsen T, Kjær C, Stenersen J (2003) Toxicity of eight polycyclic aromatic compounds to red clover (Trifolium pratense), ryegrass (Lolium perenne), and mustard (Sinapis alba). Chemosphere 53:993–1003CrossRefPubMedGoogle Scholar
  29. Verma H, Kumar R, Oldach P, Sangwan N, Khurana JP, Gilbert JA, Lal R (2014) Comparative genomic analysis of nine Sphingobium strains: insights into their evolution and hexachlorocyclohexane (HCH) degradation pathways. BMC Genomics 15:1014. doi: 10.1186/1471-2164-15-1014 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Yi H, Crowley DE (2007) Biostimulation of PAH degradation with plants containing high concentrations of linoleic acid. Environ Sci Technol 41:4382–4388CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Environmental Protection Department, Estación Experimental del ZaidínConsejo Superior de Investigaciones CientíficasGranadaSpain
  2. 2.Molecular Biology DepartmentUniversidad Nacional de Río Cuarto (UNRC)CórdobaArgentina

Personalised recommendations